Facial expression and eye gaze provide a shared signal about threats. While a fear expression with averted gaze clearly points to the source of threat, direct-gaze fear renders the source of threat ambiguous. Separable routes have been proposed to mediate these processes, with preferential attunement of the magnocellular (M) pathway to clear threat, and of the parvocellular (P) pathway to threat ambiguity. Here we investigated how observers’ trait anxiety modulates M- and P-pathway processing of clear and ambiguous threat cues. We scanned subjects (N = 108) widely ranging in trait anxiety while they viewed fearful or neutral faces with averted or directed gaze, with the luminance and color of face stimuli calibrated to selectively engage M- or P-pathways. Higher anxiety facilitated processing of clear threat projected to M-pathway, but impaired perception of ambiguous threat projected to P-pathway. Increased right amygdala reactivity was associated with higher anxiety for M-biased averted-gaze fear, while increased left amygdala reactivity was associated with higher anxiety for P-biased, direct-gaze fear. This lateralization was more pronounced with higher anxiety. Our findings suggest that trait anxiety differentially affects perception of clear (averted-gaze fear) and ambiguous (direct-gaze fear) facial threat cues via selective engagement of M and P pathways and lateralized amygdala reactivity.

In crowds, where scrutinizing individual facial expressions is inefficient, humans can make snap judgments about the prevailing mood by reading “crowd emotion”. We investigated how the brain accomplishes this feat in a set of behavioral and fMRI studies. Participants were asked to either avoid or approach one of two crowds of faces presented in the left and right visual hemifields. Perception of crowd emotion was improved when crowd stimuli contained goal-congruent cues and was highly lateralized to the right hemisphere. The dorsal visual stream was preferentially activated in crowd emotion processing, with activity in the intraparietal sulcus and superior frontal gyrus predicting perceptual accuracy for crowd emotion perception, whereas activity in the fusiform cortex in the ventral stream predicted better perception of individual facial expressions. Our findings thus reveal significant behavioral differences and differential involvement of the hemispheres and the major visual streams in reading crowd versus individual face expressions.

Fearful faces convey threat cues whose meaning is contextualized by eye gaze: While averted gaze is congruent with facial fear (both signal avoidance), direct gaze (an approach signal) is incongruent with it. We have previously shown using fMRI that the amygdala is engaged more strongly by fear with averted gaze during brief exposures. However, the amygdala also responds more to fear with direct gaze during longer exposures. Here we examined previously unexplored brain oscillatory responses to characterize the neurodynamics and connectivity during brief (~250 ms) and longer (~883 ms) exposures of fearful faces with direct or averted eye gaze. We performed two experiments: one replicating the exposure time by gaze direction interaction in fMRI (N = 23), and another where we confirmed greater early phase locking to averted-gaze fear (congruent threat signal) with MEG (N = 60) in a network of face processing regions, regardless of exposure duration. Phase locking to direct-gaze fear (incongruent threat signal) then increased significantly for brief exposures at ~350 ms, and at ~700 ms for longer exposures. Our results characterize the stages of congruent and incongruent facial threat signal processing and show that stimulus exposure strongly affects the onset and duration of these stages.

During face perception, we integrate facial expression and eye gaze to take advantage of their shared signals. For example, fear with averted gaze provides a congruent avoidance cue, signaling both threat presence and its location, whereas fear with direct gaze sends an incongruent cue, leaving threat location ambiguous. It has been proposed that the processing of different combinations of threat cues is mediated by dual processing routes: reflexive processing via magnocellular (M) pathway and reflective processing via parvocellular (P) pathway. Because growing evidence has identified a variety of sex differences in emotional perception, here we also investigated how M and P processing of fear and eye gaze might be modulated by observer's sex, focusing on the amygdala, a structure important to threat perception and affective appraisal. We adjusted luminance and color of face stimuli to selectively engage M or P processing and asked observers to identify emotion of the face. Female observers showed more accurate behavioral responses to faces with averted gaze and greater left amygdala reactivity both to fearful and neutral faces. Conversely, males showed greater right amygdala activation only for M-biased averted-gaze fear faces. In addition to functional reactivity differences, females had proportionately greater bilateral amygdala volumes, which positively correlated with behavioral accuracy for M-biased fear. Conversely, in males only the right amygdala volume was positively correlated with accuracy for M-biased fear faces. Our findings suggest that M and P processing of facial threat cues is modulated by functional and structural differences in the amygdalae associated with observer's sex.

Multiple mental disorders have been associated with dysregulation of precise brain processes. However, few therapeutic approaches can correct such specific patterns of brain activity. Since the late 1960s and early 1970s, many researchers have hoped that this feat could be achieved by closed-loop brain imaging approaches, such as neurofeedback, that aim to modulate brain activity directly. However, neurofeedback never gained mainstream acceptance in mental health, in part due to methodological considerations. In this review, we argue that, when contemporary methodological guidelines are followed, neurofeedback is one of the few intervention methods in psychology that can be assessed in double-blind placebo-controlled trials. Furthermore, using new advances in machine learning and statistics, it is now possible to target very precise patterns of brain activity for therapeutic purposes. We review the recent literature in functional magnetic resonance imaging neurofeedback and discuss current and future applications to mental health. Expected final online publication date for the Annual Review of Clinical Psychology, Volume 18 is May 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Fearful faces convey threat cues whose meaning is contextualized by eye gaze: While averted gaze is congruent with facial fear (both signal avoidance), direct gaze is incongruent with it, as direct gaze signals approach. We have previously shown using fMRI that the amygdala is engaged more strongly by fear with averted gaze, which has been found to be processed more efficiently, during brief exposures. However, the amygdala also responds more to fear with direct gaze during longer exposures. Here we examined previously unexplored brain oscillatory responses to characterize the neurodynamics and connectivity during brief (~250 ms) and longer (~883 ms) exposures of fearful faces with direct or averted eye gaze. We replicated the exposure time by gaze direction interaction in fMRI (N=23), and observed greater early phase locking to averted-gaze fear (congruent threat signal) with MEG (N=60) in a network of face processing regions, with both brief and longer exposures. Phase locking to direct-gaze fear (incongruent threat signal) then increased significantly for brief exposures at ~350 ms, and at ~700 ms for longer exposures. Our results characterize the stages of congruent and incongruent facial threat signal processing and show that stimulus exposure strongly affects the onset and duration of these stages.

Human faces evolved to signal emotions, with their meaning contextualized by eye gaze. For instance, a fearful expression paired with averted gaze clearly signals both presence of threat and its probable location. Conversely, direct gaze paired with facial fear leaves the source of the fear-evoking threat ambiguous. Given that visual perception occurs in parallel streams with different processing emphases, our goal was to test a recently developed hypothesis that clear and ambiguous threat cues would differentially engage the magnocellular (M) and parvocellular (P) pathways, respectively. We employed two-tone face images to characterize the neurodynamics evoked by stimuli that were biased toward M or P pathways. Human observers (N = 57) had to identify the expression of fearful or neutral faces with direct or averted gaze while their magnetoencephalogram was recorded. Phase locking between the amygdaloid complex, orbitofrontal cortex (OFC) and fusiform gyrus increased early (0–300 ms) for M-biased clear threat cues (averted-gaze fear) in the -band (13–30 Hz) while P-biased ambiguous threat cues (direct-gaze fear) evoked increased (4–8 Hz) phase locking in connections with OFC of the right hemisphere. We show that M and P pathways are relatively more sensitive toward clear and ambiguous threat processing, respectively, and characterize the neurodynamics underlying emotional face processing in the M and P pathways.

BackgroundTreatment attrition rates can be high for specific phobia, partly due to the subjectively aversive nature of exposure therapy that involves direct exposure to fear- and panic-inducing stimuli. A new closed-loop fMRI method called multi-voxel neuro-reinforcement has the potential to alleviate the subjective aversiveness of interventions by directly inducing phobic representations in the brain, outside of conscious awareness. The current study seeks to test this method as an intervention for specific phobia.MethodsIn a pre-registered clinical trial, individuals (N=18) with at least two animal subtype specific phobias underwent double-blind multi-voxel neuro-reinforcement for one of the two feared animals, with the untargeted one serving as control. Unaware of the target of neuro-reinforcement (i.e., the target animal), participants were guided with visual feedback and rewarded for implicit activation of the target representation. Amygdala response to phobic stimuli was assessed pre-treatment and post-treatment using photographic image presentations. Attentional capture to phobic stimuli was assessed using an affective Stroop task.ResultsConfirming our pre-registered hypothesis, a significant interaction between phobia type (target/control) and time (pre-treatment/post-treatment) was found for amygdala response. There was also a nonsignificant trend (p=0.055) for the hypothesized attentional capture during the affective Stroop. In both measures, responding to the phobia targeted with neuro-reinforcement was selectively reduced compared to the placebo control.ConclusionsResults suggest multi-voxel neuro-reinforcement has the potential to be a successful intervention for specific phobia. Multi-voxel neuro-reinforcement decreased physiological and behavioral responses to specific phobia through reduced amygdala activation and attentional capture by phobic stimuli. Consequently, multi-voxel neuro-reinforcement may complement current conventional psychotherapy approaches while providing a non-distressing experience for patients seeking treatment.